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Zootaxa, Integrative Taxonomy Identifies New (And Old) Species In Zootaxa 2032: 1–38 (2009) ISSN 1175-5326 (print edition) www.mapress.com/zootaxa/ Article ZOOTAXA Copyright © 2009 · Magnolia Press ISSN 1175-5334 (online edition) Integrative taxonomy identifies new (and old) species in the Lasioglossum (Dialictus) tegulare (Robertson) species group (Hymenoptera, Halictidae) JASON GIBBS York University, Department of Biology, 4700 Keele St., Toronto, Ontario, M3J1P3, Canada. E-mail: [email protected] Table Of Contents Abstract ............................................................................................................................................................................... 1 Introduction ......................................................................................................................................................................... 2 Materials and methods ........................................................................................................................................................ 3 Results ................................................................................................................................................................................. 5 Lasioglossum (Dialictus) tegulare species group...................................................................................................... 13 Lasioglossum (Dialictus) tegulare (Robertson), comb. n. ........................................................................................ 13 Lasioglossum (Dialictus) ellisiae (Sandhouse), comb. n. ......................................................................................... 18 Lasioglossum (Dialictus) lepidii (Graenicher), comb. n............................................................................................ 22 Lasioglossum (Dialictus) puteulanum Gibbs, sp. n. .................................................................................................. 25 Lasioglossum (Dialictus) carlinvillense Gibbs, sp. n................................................................................................ 28 Key to eastern species ....................................................................................................................................................... 32 Discussion ......................................................................................................................................................................... 32 Acknowledgements ........................................................................................................................................................... 34 Literature cited .................................................................................................................................................................. 35 Abstract An integrative taxonomic approach that utilizes the DNA barcode region of cytochrome c oxidase subunit 1 in conjunction with traditional morphological approaches identifies five distinct species previously recognized as Lasioglossum (Dialictus) tegulare (Robertson). Differences in DNA sequences and congruent, albeit minor, morphological variation support separation of L. tegulare into five species. Unique nucleotide substitution patterns for each species allows for character-based diagnostics using DNA barcodes. The names L. ellisiae (Sandhouse) and L. lepidii (Graenicher) are removed from synonymy. Two new species, L. puteulanum Gibbs sp. n. and L. carlinvillense Gibbs sp. n., are described. A key is provided, which permits the identification of both males and females. The utility of the DNA barcode region as part of an integrative taxonomic framework is discussed. Key words: Cryptic species, integrative taxonomy, DNA barcodes, Lasioglossum, Dialictus, Halictidae Accepted by E. Almeida: 20 Feb. 2009; published: 11 Mar. 2009 1 Introduction Several methods for automated species identification using quantitative approaches have been proposed (Gaston & O’Neill 2004) but none has garnered the attention of DNA barcoding. DNA barcoding is a new method that promises to speed taxonomic progress and allow identification of specimens even without taxonomic expertise (Hebert et al. 2003a). DNA barcoding employs a short strand of a standard gene to identify species. A 657-bp fragment of the mitochondrial cytochrome c oxidase subunit I (COI) is the chosen standard for animals (Hebert et al. 2003a). DNA barcoding has incited much controversy in the taxonomic community and has been both lauded and denounced in the literature (e.g. Trewick 2008 and references therein). Integrative taxonomic approaches that combine morphological, molecular and other types of data are the best methods for describing species (Dayrat 2005; Page et al. 2005; DeSalle et al. 2005). Morphological and molecular data have complementary strengths (Hillis 1987; Hillis & Wiens 2000) and in combination can overcome weaknesses of single datasets alone (e.g. Wahlberg et al. 2005). Molecular evidence can provide an independent test of morphological assessments of species identity and vice versa (Page et al. 2005). Multiple sources of data (e.g. morphology, DNA, geography) are needed to test and corroborate hypothetical species limits (DeSalle et al. 2005). DNA barcoding efforts provide molecular data that may aid in discovering cryptic species (Hebert et al. 2004; Yassin et al. 2007) but these findings should be incorporated into an integrative taxonomic framework (Dayrat 2005; DeSalle et al. 2005). Confounding factors such as incomplete lineage sorting or diversifying selection acting on morphological traits can result in closely related species that cannot be differentiated by a single piece of molecular evidence (Avise 2000; Funk & Omland 2003). In this respect, the DNA barcode region does not differ from other candidate genes. DNA barcoding efforts are novel relative to other molecular methods by virtue of the standardization and taxonomic breadth for which DNA sequence data is being made available. One advantage of selecting the DNA barcode region for integrative taxonomic purposes over other genes is that the data can be used both for alpha taxonomy and for species identification. The importance of bees as pollinators (Buchmann & Nabhan 1996; Klein et al. 2007) and their potential as ecosystem monitors (Zayed et al. 2004) makes their study of particular importance. The large number of bee species (>19,000 valid species-names worldwide [Ascher et al. 2008]) with many highly speciose genera and subgenera makes species recognition difficult. In many cases, cryptic species, caste differentiation and sexual dimorphism add to the puzzle (Sandhouse 1924; Knerer & Atwood 1962; Janjic & Packer 2001; Pilgrim & Pitts 2006; Sheffield & Westby 2007). Molecular evidence, such as DNA barcodes, may not only differentiate cryptic species (Carman & Packer 1997; Packer & Taylor 1997; Danforth et al. 1998; Hebert et al. 2004; Witt et al. 2006; see Avise 2000, 2004 for further examples) but also associate queens, workers, larval stages and dimorphic sexes (Pilgrim & Pitts 2006; Gibbs in press) that would otherwise be misidentified (or not identified further than subgenus) based on morphology alone. The subgenus Dialictus (Halictidae: Lasioglossum) is one of the most taxonomically difficult groups amongst the bees. In North America, Dialictus are both speciose (over 270 currently recognized names) and the most commonly collected subgenus of bee (MacKay & Knerer 1979; Eickwort 1988; Grixti & Packer 2006; Campbell et al. 2007). Dialictus are also notoriously difficult to identify to species because they are “morphologically monotonous” (Packer 1997; Michener 2007). In most cases, only very subtle differences can be used to differentiate closely related species. Identification is further complicated by the existence of castes in the many eusocial species (reviewed in Michener 1974; Packer 1993; Yanega 1997). In bee diversity studies many Dialictus cannot be identified to the species level (e.g. Giles & Ascher 2006) preventing more in depth study of sociobiology, biodiversity and pollination biology. The extreme similarity between species may be due in part to a recent origin and rapid diversification of the speciose lineage containing Dialictus, likely to have started 20–22 million years ago (Brady et al. 2006). Very little taxonomic progress has been made on this group in the last forty years (Mitchell 1960; Knerer & Atwood 1966), and there is much work to be done. The nominal species Lasioglossum tegulare (Robertson), widespread in eastern North America, is one of 2 · Zootaxa 2032 © 2009 Magnolia Press GIBBS the few currently recognized species of Dialictus that is easy to identify. As the name suggests, this species has a distinctive tegula (Fig. 1), which is remarkable for its size, shape and punctation. Two additional species from the eastern United States, L. marinum (Crawford) and L. surianae (Mitchell), have similar tegulae but are easily distinguished morphologically from L. tegulare. The microsculpture of L. tegulare, as well as its size and colouration, differ from L. marinum and the two are not close relatives (Gibbs, unpublished data). Lasioglossum surianae has distinct colouration patterns that easily distinguish it from L. tegulare. The presence of the elongate tegula was not mentioned in Mitchell’s (1960) key or description of L. surianae but inspection of the holotype clearly shows this character. Lasioglossum marinum is a sand dune specialist uncommonly collected outside of coastal areas from Florida
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